Skip to main content

Advertisement

Log in

Bacterial Activity, Community Structure, and Centimeter-Scale Spatial Heterogeneity in Contaminated Soil

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

In an anthropogenically disturbed soil (88% sand, 8% silt, 4% clay), 150-mg samples were studied to examine the fine-scale relationship of bacterial activity and community structure to heavy metal contaminants. The soils had been contaminated for over 40 years with aromatic solvents, Pb, and Cr. Samples from distances of <1, 5, 15, and 50 cm over a depth range of 40–90 cm underwent a sequential analysis to determine metabolic potential (from 14C glucose mineralization), bacterial community structure [using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE)], and total extractable Pb and Cr levels. Metabolic potential varied by as much as 10,000-fold in samples <1 cm apart; log–log plots of metal concentration and microbial metabolic potential showed no correlation with each other. Overall, metal concentrations ranged from 9 to 29,000 mg kg−1 for Pb and from 3 to 8500 mg kg−1 for Cr with small zones of high contamination present. All regions exhibited variable metal concentrations, with some soil samples having 30-fold differences in metal concentration in sites <1 cm apart. Geostatistical analysis revealed a strong spatial dependence for all three parameters tested (metabolic activity, Pb, and Cr levels) with a range up to 30 cm. Kriging maps showed that in zones of high metal, the corresponding metabolic activity was low suggesting that metals negatively impacted the microbial community. PCR-DGGE analysis revealed that diverse communities were present in the soils with a random distribution of phylotypes throughout the sampling zones. These results suggest the presence of spatially isolated microbial communities within the soil profile.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389–3402 Occurrence Handle10.1093/nar/25.17.3389 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D Occurrence Handle9254694

    Article  CAS  PubMed  Google Scholar 

  2. Beasley, F (2004) Characterization of diversity, chromate resistance, and aromatic hydrocarbon degradation among Arthrobacter isolates from mixed waste soil. MS dissertation, Purdue University, West Lafayette

  3. Y Benjamini Y Hochberg (1995) ArticleTitleControlling the false discovery rate—a practical and powerful approach to multiple testing J R Stat Soc, B 57 289–300

    Google Scholar 

  4. SJ Bent CL Gucker Y Oda LJ Forney (2003) ArticleTitleSpatial distribution of Rhodopseudomonas palustris ecotypes on a local scale Appl Environ Microbiol 69 5192–5197 Occurrence Handle10.1128/AEM.69.9.5192-5197.2003 Occurrence Handle1:CAS:528:DC%2BD3sXntlSjtLg%3D Occurrence Handle12957901

    Article  CAS  PubMed  Google Scholar 

  5. TD Brock (1978) ArticleTitleUse of fluorescence microscopy for quantifying phytoplankton, especially filamentous blue-green algae Limnol Oceanogr 23 158–160

    Google Scholar 

  6. JM Coombs T Barkay (2004) ArticleTitleMolecular evidence for the evolution of metal homeostasis genes by lateral gene transfer in bacteria from the deep terrestrial subsurface Appl Environ Microbiol 70 1698–1707 Occurrence Handle10.1128/AEM.70.3.1698-1707.2004 Occurrence Handle1:CAS:528:DC%2BD2cXisVKisL4%3D Occurrence Handle15006795

    Article  CAS  PubMed  Google Scholar 

  7. M Díaz-Raviña E Bååth (1996) ArticleTitleDevelopment of metal tolerance in soil bacterial communities exposed to experimentally increased metal levels Appl Environ Microbiol 62 2970–2977

    Google Scholar 

  8. M Díaz-Raviña E Bååth (2001) ArticleTitleResponse of soil bacterial communities pre-exposed to different metals and reinoculated in an unpolluted soil Soil Biol Biochem 33 241–248 Occurrence Handle10.1016/S0038-0717(00)00136-X

    Article  Google Scholar 

  9. M Díaz-Raviña E Bååth Å Frostegård (1994) ArticleTitleMultiple heavy metal tolerance of soil bacterial communities and its measurement by a thymidine incorporation technique Appl Environ Microbiol 60 2238–2247 Occurrence Handle16349314

    PubMed  Google Scholar 

  10. CH Ettema DA Wardle (2002) ArticleTitleSpatial soil ecology Trends Ecol Evol 17 177–183 Occurrence Handle10.1016/S0169-5347(02)02496-5

    Article  Google Scholar 

  11. A Felske ADL Akkermans (1998) ArticleTitleSpatial homogeneity of abundant bacterial 16S rRNA molecules in grassland soils Microb Ecol 36 31–36 Occurrence Handle10.1007/s002489900090 Occurrence Handle1:CAS:528:DyaK1cXksVOrurs%3D Occurrence Handle9622562

    Article  CAS  PubMed  Google Scholar 

  12. K Feris P Ramsey C Frazar JN Moore JE Gannon WE Holben (2003) ArticleTitleDifferences in hyporheic-zone microbial community structure along a heavy-metal contamination gradient Appl Environ Microbiol 69 5563–5573 Occurrence Handle10.1128/AEM.69.9.5563-5573.2003 Occurrence Handle1:CAS:528:DC%2BD3sXntlSis7w%3D Occurrence Handle12957946

    Article  CAS  PubMed  Google Scholar 

  13. KP Feris PW Ramsey M Rillig JN Moore JE Gannon WE Holben (2004) ArticleTitleDetermining rates of change and evaluating group-level resiliency differences in hyporheic microbial communities in response to fluvial heavy-metal deposition Appl Environ Microbiol 70 4756–4765 Occurrence Handle1:CAS:528:DC%2BD2cXms1elu78%3D Occurrence Handle15294812

    CAS  PubMed  Google Scholar 

  14. A Fließbach R Martens HH Reber (1994) ArticleTitleSoil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage sludge Soil Biol Biochem 26 1201–1205 Occurrence Handle10.1016/0038-0717(94)90144-9

    Article  Google Scholar 

  15. RB Franklin LK Blum AC McComb AL Mills (2002) ArticleTitleA geostatistical analysis of small-scale spatial variability in bacterial abundance and community structure in salt marsh creek bank sediments FEMS Microbiol Ecol 42 71–80 Occurrence Handle1:CAS:528:DC%2BD38Xnt1KmtL4%3D Occurrence Handle12542032

    CAS  PubMed  Google Scholar 

  16. RB Franklin AL Mills (2003) ArticleTitleMulti-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field FEMS Microbiol Ecol 44 335–346 Occurrence Handle1:CAS:528:DC%2BD3sXjs1Ckurk%3D Occurrence Handle12830827

    CAS  PubMed  Google Scholar 

  17. Å Frostegård A Tunlid E Bååth (1996) ArticleTitleChanges in microbial community structure during long-term incubation in two soils experimentally contaminated with metals Soil Biol Biochem 28 55–63 Occurrence Handle10.1016/0038-0717(95)00100-X

    Article  Google Scholar 

  18. Å Frostegård A Tunlid E Bååth (1993) ArticleTitlePhospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals Appl Environ Microbiol 59 3605–3617 Occurrence Handle16349080

    PubMed  Google Scholar 

  19. LV Gonod C Chenu G Soulas (2003) ArticleTitleSpatial variability of 2,4-dichlorophenoxyacetic acid (2,4-D) mineralisation potential at a millimetre scale in soil Soil Biol Biochem 35 373–382 Occurrence Handle10.1016/S0038-0717(02)00287-0 Occurrence Handle1:CAS:528:DC%2BD3sXhvFGrtr0%3D

    Article  CAS  Google Scholar 

  20. JH Görres MJ Dichiaro JB Lyons JA Amador (1998) ArticleTitleSpatial and temporal patterns of soil biological activity in a forest and an old field Soil Biol Biochem 30 219–230

    Google Scholar 

  21. BS Griffiths M Díaz-Raviña K Ritz JW McNicol N Ebblewhite N Bååth (1997) ArticleTitleCommunity DNA hybridisation and %G + C profiles of microbial communities from heavy metal polluted soils FEMS Microbiol Ecol 24 103–112 Occurrence Handle1:CAS:528:DyaK2sXmsl2ns78%3D

    CAS  Google Scholar 

  22. GL Grundmann D Debouzie (2000) ArticleTitleGeostatistical analysis of the distribution of NH4+ and NO2-oxidizing bacteria and serotypes at the millimeter scale along a soil transect FEMS Microbiol Ecol 34 57–62 Occurrence Handle1:CAS:528:DC%2BD3cXosVyrtLw%3D Occurrence Handle11053736

    CAS  PubMed  Google Scholar 

  23. GL Grundmann A Dechesne F Bartoli JP Flandrois JL Chasse R Kizungu (2001) ArticleTitleSpatial modeling of nitrifier microhabitats in soil Soil Sci Soc Am J 65 1709–1716 Occurrence Handle1:CAS:528:DC%2BD38Xht1SmurY%3D

    CAS  Google Scholar 

  24. GL Grundmann P Normand (2000) ArticleTitleMicroscale diversity of the genus Nitrobacter in soil on the basis of analysis of genes encoding rRNA Appl Environ Microbiol 66 4543–4546 Occurrence Handle10.1128/AEM.66.10.4543-4546.2000 Occurrence Handle1:CAS:528:DC%2BD3cXnt1Cls78%3D Occurrence Handle11010914

    Article  CAS  PubMed  Google Scholar 

  25. SP Hubbell (2001) The Unified Theory of Biodiversity and Biogeography Princeton University Press Princeton, NJ

    Google Scholar 

  26. E Kandeler D Tscherko KD Bruce M Stemmer PJ Hobbs RD Bardgett W Amelung (2000) ArticleTitleStructure and function of the soil microbial community in microhabitats of a heavy metal polluted soil Biol Fertil Soils 32 390–400 Occurrence Handle10.1007/s003740000268 Occurrence Handle1:CAS:528:DC%2BD3cXosVSjtLY%3D

    Article  CAS  Google Scholar 

  27. JJ Kelly M Häggblom RL Tate SuffixIII (1999) ArticleTitleChanges in soil microbial communities over time resulting from one time application of zinc: a laboratory microcosm study Soil Biol Biochem 31 1455–1465 Occurrence Handle1:CAS:528:DyaK1MXltVOks7Y%3D

    CAS  Google Scholar 

  28. M Khan J Scullion (2000) ArticleTitleEffect of soil on microbial responses to metal contamination Environ Pollut 110 115–125 Occurrence Handle10.1016/S0269-7491(99)00288-2 Occurrence Handle1:CAS:528:DC%2BD3cXksFyiur0%3D Occurrence Handle15092861

    Article  CAS  PubMed  Google Scholar 

  29. J Kozdrój JD Elsas Particlevan (2001) ArticleTitleStructural diversity of microbial communities in arable soils of a heavily industrialised area determined by PCR-DGGE fingerprinting and FAME profiling Appl Soil Ecol 17 31–42 Occurrence Handle10.1016/S0929-1393(00)00130-X

    Article  Google Scholar 

  30. L Leita MD Nobili G Muhlbachova C Mondini L Marchiol G Zerbi (1995) ArticleTitleBioavailabilty and effects of heavy-metals on soil microbial biomass survival during laboratory incubation Biol Fertil Soils 19 103–108 Occurrence Handle10.1007/BF00336144 Occurrence Handle1:CAS:528:DyaK2MXkvVCkt7c%3D

    Article  CAS  Google Scholar 

  31. SJ Morris (1999) ArticleTitleSpatial distribution of fungal and bacterial biomass in southern Ohio hardwood forest soils: fine scale variability and microscale patterns Soil Biol Biochem 31 1375–1386 Occurrence Handle1:CAS:528:DyaK1MXltVOks74%3D

    CAS  Google Scholar 

  32. DL Mummey PD Stahl (2004) ArticleTitleAnalysis of soil whole- and inner-microaggregate bacterial communities Microb Ecol 48 41–50 Occurrence Handle10.1007/s00248-003-1000-4 Occurrence Handle1:STN:280:DC%2BD2cvovVKgug%3D%3D Occurrence Handle15085298

    Article  CAS  PubMed  Google Scholar 

  33. G Muyzer EC Waal Particlede AG Uitterlinden (1993) ArticleTitleProfiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA Appl Environ Microbiol 59 695–700 Occurrence Handle1:CAS:528:DyaK3sXit1Kktrk%3D Occurrence Handle7683183

    CAS  PubMed  Google Scholar 

  34. S Nazaret E Brothier L Ranjard (2003) ArticleTitleShifts in diversity and microscale distribution of the adapted bacterial phenotypes due to Hg(II) spiking in soil Microb Ecol 45 259–269 Occurrence Handle10.1007/s00248-002-2035-7 Occurrence Handle1:CAS:528:DC%2BD3sXkvFGls7Y%3D Occurrence Handle12658524

    Article  CAS  PubMed  Google Scholar 

  35. DR Nielsen O Wendroth (2003) Spatial and Temporal Statistics: sampling Field Soils and Their Vegetation Catena Verlag, GmbH Reiskirchen

    Google Scholar 

  36. N Nunan K Wu IM Young JW Crawford K Ritz (2002) ArticleTitleIn situ spatial patterns of soil bacterial populations, mapped at multiple scales, in an arable soil Microb Ecol 44 296–305 Occurrence Handle10.1007/s00248-002-2021-0 Occurrence Handle1:STN:280:DC%2BD38jhtFOmug%3D%3D Occurrence Handle12375095

    Article  CAS  PubMed  Google Scholar 

  37. TB Parkin (1993) ArticleTitleSpatial variability of microbial processes in soil—a review J Environ Qual 22 409–417

    Google Scholar 

  38. T Pennanen Å Frostegård H Fritze E Bååth (1996) ArticleTitlePhospholipid fatty acid composition and heavy metal tolerance of soil microbial communities along two heavy metal-polluted gradients in coniferous forests Appl Environ Microbiol 62 420–428 Occurrence Handle1:CAS:528:DyaK28XovVCmug%3D%3D

    CAS  Google Scholar 

  39. L Ranjard E Brothier S Nazaret (2000) ArticleTitleSequencing bands of ribosomal intergenic spacer analysis fingerprints for characterization andmicroscale distribution of soil bacterium populations responding to mercury spiking Appl Environ Microbiol 66 5334–5339 Occurrence Handle10.1128/AEM.66.12.5334-5339.2000 Occurrence Handle1:CAS:528:DC%2BD3MXjsVyhu7c%3D Occurrence Handle11097911

    Article  CAS  PubMed  Google Scholar 

  40. L Ranjard S Nazaret F Gourbière J Thioulouse P Linet A Richaume (2000) ArticleTitleA soil microscale study to reveal the heterogeneity of Hg(II) impact on indigenous bacteria by quantification of adapted phenotypes and analysis of community DNA fingerprints FEMS Microbiol Ecol 31 107–115 Occurrence Handle1:CAS:528:DC%2BD3cXltVCmug%3D%3D Occurrence Handle10640664

    CAS  PubMed  Google Scholar 

  41. L Ranjard A Richaume (2001) ArticleTitleQuantitative and qualitative microscale distribution of bacteria in soil Res Microbiol 152 707–716 Occurrence Handle10.1016/S0923-2508(01)01251-7 Occurrence Handle1:STN:280:DC%2BD3Mnht1SqsQ%3D%3D Occurrence Handle11686384

    Article  CAS  PubMed  Google Scholar 

  42. L Ranjard A Richaume L Jocteur-Monrozier S Nazaret (1997) ArticleTitleResponse of soil bacteria to Hg(II) in relation to soil characteristics and cell location FEMS Microbiol Ecol 24 321–331 Occurrence Handle1:CAS:528:DyaK2sXotVyjtLk%3D

    CAS  Google Scholar 

  43. LD Rasmussen SJ Sørensen (1998) ArticleTitleThe effect of long-term exposure to mercury on the bacterial community in marine sediment Curr Microbiol 36 291–297 Occurrence Handle10.1007/s002849900312 Occurrence Handle1:CAS:528:DyaK1cXislWjsLc%3D Occurrence Handle9541566

    Article  CAS  PubMed  Google Scholar 

  44. K Ritz JW McNicol N Nunan S Grayston P Millard D Atkinson D Gollotte D Habeshaw B Boag CD Clegg BS Griffiths RE Wheatley LA Glover AE McCaig JI Prosser (2004) ArticleTitleSpatial structure in soil chemical and microbiological properties in an upland grassland FEMS Microbiol Ecol 49 191–205 Occurrence Handle1:CAS:528:DC%2BD2cXlsl2iur0%3D

    CAS  Google Scholar 

  45. RE Rossi DJ Mulla AG Journel EH Franz (1992) ArticleTitleGeostatistical tools for modeling and interpreting ecological spatial dependence Ecol Monogr 62 297–314

    Google Scholar 

  46. P Saetre E Bååth (2000) ArticleTitleSpatial variation and patterns of soil microbial community structure in a mixed spruce–birch stand Soil Biol Biochem 32 909–917 Occurrence Handle10.1016/S0038-0717(99)00215-1 Occurrence Handle1:CAS:528:DC%2BD3cXltVCrur4%3D

    Article  CAS  Google Scholar 

  47. R-A Sandaa V Torsvik Ø Enger (2001) ArticleTitleInfluence of long-term heavy-metal contamination on microbial communities in soil Soil Biol Biochem 33 287–295 Occurrence Handle10.1016/S0038-0717(00)00139-5 Occurrence Handle1:CAS:528:DC%2BD3MXhslKls7s%3D

    Article  CAS  Google Scholar 

  48. R-A Sandaa V Torsvik Ø Enger FL Daae T Castberg D Hahn (1999) ArticleTitleAnalysis of bacterial communities in heavy-metal contaminated soil at different levels of resolution FEMS Microbiol Ecol 30 237–251 Occurrence Handle1:CAS:528:DyaK1MXmsFahs78%3D Occurrence Handle10525180

    CAS  PubMed  Google Scholar 

  49. A Sessitsch A Weilharter MH Gerzabek H Kirchmann E Kandeler (2001) ArticleTitleMicrobial population structures in soil particle size fractions of a long-term fertilizer field experiment Appl Environ Microbiol 67 4215–4224 Occurrence Handle10.1128/AEM.67.9.4215-4224.2001 Occurrence Handle1:CAS:528:DC%2BD3MXmslWisL0%3D Occurrence Handle11526026

    Article  CAS  PubMed  Google Scholar 

  50. W Shi M Bischoff R Turco A Konopka (2002) ArticleTitleLong-term effects of chromium and lead upon the activity of soil microbial communities Appl Soil Ecol 21 169–177 Occurrence Handle10.1016/S0929-1393(02)00062-8

    Article  Google Scholar 

  51. MK Sliwinski RM Goodman (2004) ArticleTitleSpatial heterogeneity of Crenarchaeal assemblages within mesophilic soil ecosystems as revealed by PCR-single-stranded conformation polymorphism profiling Appl Environ Microbiol 70 1811–1820 Occurrence Handle1:CAS:528:DC%2BD2cXisVKisb0%3D Occurrence Handle15006808

    CAS  PubMed  Google Scholar 

  52. V Torsvik L Øvreås TF Thingstad (2002) ArticleTitleProkaryotic diversity—magnitude, dynamics, and controlling factors Science 296 1064–1066 Occurrence Handle10.1126/science.1071698 Occurrence Handle1:CAS:528:DC%2BD38Xjslantrc%3D Occurrence Handle12004116

    Article  CAS  PubMed  Google Scholar 

  53. DS Treves B Xia J Zhou JM Tiedje (2003) ArticleTitleA two-species test of the hypothesis that spatial isolation influences microbial diversity in soil Microb Ecol 45 20–28 Occurrence Handle10.1007/s00248-002-1044-x Occurrence Handle1:STN:280:DC%2BD3s%2FmsVWltw%3D%3D Occurrence Handle12415419

    Article  CAS  PubMed  Google Scholar 

  54. R Turpeinen T Kairesalo M Häggblom (2004) ArticleTitleMicrobial community structure and activity in arsenic-, chromium- and copper-contaminated soils FEMS Microbiol Ecol 47 39–50 Occurrence Handle1:CAS:528:DC%2BD2cXltVyntg%3D%3D

    CAS  Google Scholar 

  55. B Xia DS Treves J Zhou JM Tiedje (2001) ArticleTitleSoil microbial community diversity and driving mechanisms Prog Nat Sci 11 818–824

    Google Scholar 

  56. H Yao J Xu C Huang (2003) ArticleTitleSubstrate utilization pattern, biomass and activity of microbial communities in a sequence of heavy metal-polluted paddy soils Geoderma 115 139–148 Occurrence Handle10.1016/S0016-7061(03)00083-1 Occurrence Handle1:CAS:528:DC%2BD3sXjvVCls7Y%3D

    Article  CAS  Google Scholar 

  57. J Zhou B Xia H Huang AV Palumbo JM Tiedje (2004) ArticleTitleMicrobial diversity and heterogeneity in sandy subsurface soils Appl Environ Microbiol 70 1723–1734 Occurrence Handle1:CAS:528:DC%2BD2cXisVKisL0%3D Occurrence Handle15006798

    CAS  PubMed  Google Scholar 

  58. J Zhou B Xia DS Treves L-Y Wu TL Marsh RV O'Neill AV Palumbo JM Tiedje (2002) ArticleTitleSpatial and resource factors influencing high microbial diversity in soil Appl Environ Microbiol 68 326–334 Occurrence Handle1:CAS:528:DC%2BD38Xjt1WmtQ%3D%3D Occurrence Handle11772642

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Department of Energy's Natural and Accelerated Bioremediation Research (NABIR) program (Grant no. DE-FG02-98ER62681). Our thanks to Indiana Department of Transport and, in particular, Bill Jarvis for giving us access to thissite.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joanna M. Becker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Becker, J.M., Parkin, T., Nakatsu, C.H. et al. Bacterial Activity, Community Structure, and Centimeter-Scale Spatial Heterogeneity in Contaminated Soil. Microb Ecol 51, 220–231 (2006). https://doi.org/10.1007/s00248-005-0002-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-005-0002-9

Keywords

Navigation